Overview of the Genus Phyllactinia (Ascomycota, Erysiphales) in Azerbaijan

Home , Crataegus meyeri, Erysiphales, Morus australis, Phyllactinia, Prunus fenzliana

Plant & Fungal Research (2018) 1(1): 9-17 © The Institute of Botany, ANAS, Baku, Azerbaijan http://dx.doi.org/10.29228/plantfungalres.2 December 2018

Overview of the genus Phyllactinia (Ascomycota, Erysiphales) in Azerbaijan

Dilzara N. Aghayeva1 Key Words: distribution, ectoparasitism, endoparasit- Lamiya V. Abasova ism, host plant, plant pathogen, powdery mildews Institute of Botany, Azerbaijan National Academy of Sciences, Badamdar 40, Baku, AZ1004, Azerbaijan INTRODUCTION Susumu Takamatsu Graduate School of Bioresources, Mie University, Powdery mildews are one of the frequently encoun- 1577 Kurima-Machiya, Tsu 514-8507, Japan tered plant pathogens and most of them are epiphytic (14 genera from 18), in which they tend to produce hy- Abstract: Intergeneric diversity of powdery mildews phae and reproductive structures on surface of leaves, within the genus Phyllactinia in Azerbaijan was inves- young shoots and inflorescence [Braun, Cook, 2012; tigated using morphological approaches based on re-ex- Glawe, 2008]. These fungi absorb nutrients from plant amination of herbarium specimens kept in Mycological tissue via haustoria, which develops in epidermal cells Herbarium of the Institute of Botany (BAK), Azerbaijan of plants [Braun, Cook, 2012]. Among all powdery mil- National Academy of Sciences and collections of re- dews only four genera demonstrate endoparasitism, of cent years. To contribute detail taxonomic analysis data them Phyllactinia Lév., have partly endoparasitic na- given in literatures was revised. Modern taxonomic and ture. Fungi belonging to these genera penetrate into the nomenclature changes were considered. The host range plant cell via stomata and develop haustoria in paren- and geographical distribution of species residing to the chyma cells. Endoparasitic genera of powdery mildews genus within the country were clarified. Consequently, (Phyllactinia, Pleochaeta Sacc. & Speg., Queirozia 17 powdery mildew taxa were recorded, of which Ph. Viégas & Cardoso and Leveillula G. Arnaud) form a alnicola, Ph. ampelopsidis, Ph. babayanii, Ph. carpini, distinct monophyletic group within Erysiphales which Ph. corni, Ph. fraxini, Ph. guttata, Ph. mali, Ph. ma- suggests that endoparasitism derived from ectoparasit- rissalii, Ph. moricola, Ph. nivea, Ph. orbicularis, Ph. ism in powdery mildews only once in their evolution paliuri, Ph. phaseolina, Ph. populi, Ph. pyri-serotinae [Takamatsu, 2013; Takamatsu et al. 2016]. Only genus and Ph. roboris on 32 plant species from 11 families Leveillula exhibits true endoparasitism and elongates were listed. These families belong to the groups Aster- internal hyphae between host cells in mesophyll layer ids (Cornaceae, Oleaceae) and Rosids (Fabaceae, Betu- [Takamatsu et al. 2008, 2016]. laceae, Fagaceae, Salicaceae, Moraceae, Rhamnaceae, Phyllactinia is distinguishable from other powdery Rosaceae, Ulmaceae, Sapindaceae, Vitaceae), of which mildews based on its unique characteristics of sexual Rosids exceeds in number of host species. The family morphs, viz. large ascomata (chasmothecia) with two Rosaceae possess the large amount of host species, but different types of appendages. One of them is acicular specific affinity of genus Phyllactinia is considered to appendages with bulbous swellings at the base, which be to the family Betulaceae. In addition, Phyllactinia arise equatorially and play role in orientation of asco- powdery mildews seemed to spread mainly in moun- mata through the air during dispersal. Second one, peni- tainous areas of Azerbaijan. The highest number of taxa cillate cells composed of foots (outgrows of the asco- was recorded in the districts belonging to the Southern- matal walls), filaments [Shin, Lee, 2002] and grouped East Great Caucasus region of the country, followed by together on the dorsal surface of chasmothecia [Glawe, regions Middle Araz and Lesser Caucasus. The low- 2008]. Penicillate cells perform a role as anchor for at- est number of Phyllactinia taxa was recorded from taching of chasmothecia to the new plant surface by Kur lowland and Lankaran regions. During the present gelatinizing of filaments under humid condition [Taka- study, it was revealed that herbarium samples of 14 taxa matsu et al., 2008]. There is a speculation that unique of genus Phyllactinia are available in the BAK, infor- characteristics of appendages are an evolutionary adap- mation of which is provided in this article. tation to the tree parasitism of this genus [Takamatsu et al., 2008]. Powdery mildews from this genus form Accepted for publication: 5 December 2018 whitish to grayish colony under the leaf surface. The 1E-mail: [email protected] genus is characterized by having 2–3-spored asci, main-

9 Plant & Fungal Research ly monomorphic, sometimes dimorphic conidia with clavate, dumble-like, subcylindric, broadly ellipsoid- ovoid, lanceolate shape, almost indistinct and nipple or rod-shaped appressoria [Braun, Cook, 2012] (Fig. 1). According to the monograph of the Erysiphales, 102 species were counted within the genus Phyllactinia [Braun, Cook, 2012] and they are strictly woody parasitic fungi, which are known on about 700 plant species from 69 families [Amano, 1986]. Totally, 108 plant species from family Rosaceae were dedected as host for genus Phyllactinia and the order is followed by families Betulaceae (91 species), Fagaceae (56 species), Oleace- ae (50 species), etc. [Takamatsu et al., 2008]. The aims of this study were to reveal diversity of powdery mildews from the genus Phyllactinia, to clarify the ratio of Phyllactinia taxa within the Erysiphales in Azerbaijan, to update species composition by taking Figure 1. Phyllactinia moricola; A. acicular appendage into the consideration modern taxonomic and nomen- with bulbous swelling; B. penicillate cell, b1. foot, b2. clature changes, and to investigate their host range and filaments; C. conidia; D. conidiophores; E. appressoria; geographical distribution within country. Bar = 100 μm.

MATERIAL AND METHODS Herbarium samples kept at the Mycological Herbari- RESULTS AND DISCUSSION um of the Institute of Botany, ANAS (BAK) and new Taxonomy. Diversity of powdery mildews in Azerbaijan samples collected from 2016 to 2018 were investigated is currently represented with 134 fungal taxa from ten using classic morphological approaches. To contribute genera on 420 plant species from 51 families [Abasova, detail taxonomic investigations, literature data were Ağayeva, 2018]. The genus Erysiphe R. Hedw. ex DC. summarized. dominates by possessing the largest number of fungal Morphological examinations were done under the taxa, followed by the genus Podosphaera Kunze, Go- optical microscope (Vert. A1, Carl Zeiss, Axio Imager, lovinomyces (U.Braun) Heluta, Phyllactinia, and Lev- Göttingen, Germany). To examine asexual structures a eillula. Genera Arthrocladiella Vassilkov, Blumeria little piece of infected leaf was rehydrated using lactic Golovin ex Speer, Neoërysiphe U.Braun and Sawadaea acid method [Shin, La, 1993]. For observation of sexual Miyabe are quite small and consist of one or two species morphs, chasmothecia were mounted in 3% NaOH so- for each genus [Abasova, Ağayeva, 2018]. Intergeneric lution [Meeboon, Takamatsu, 2015]. Thirty measure- diversity of the genus Phyllactinia, their host range, ments for each structure were taken. Measurements geographical distribution within the country, and tradi- of asexual structures were done based on the length of tional names put on the specimens and BAK numbers of conidiophores, size and shape of conidia and appres- were given below. soria. For sexual structures diameter of chasmothecia, Ph. alnicola U. Braun, Braun & Cook 226, 2012; and number, size and shape of asci and ascospores were = Ph. suffulta f. alni Hammarl.; Host: Alnus glutinosa considered. Bulmer’s factor (l × 1.5; w × 1.2) was used (L.) Gaertn. (Betulaceae); BAK 5612, 5614, 5615; Dis- to reconstruct the original size of conidia for herbarium tribution: Qusar, Zaqatala (Fig.2.1). samples [Braun, Cook, 2012]. Drawings were made by Ph. ampelopsidis Y.N. Yu & Y.Q. Lai, Acta Micro- freehand using scale bar. biol. Sin. 19 (1): 14, 1979; Host: Vitis vinifera L. (Vi- Identification of fungal species was carried out by taceae); BAK 5778; Distribution: Khojavend. Previ- using the latest literature [Braun, Cook, 2012]. Nomen- ously a powdery mildew fungus on Vitis vinifera from clature changes were done according to the Mycobank Azerbaijan was described as Phyllactinia suffulta f. vi- and Index Fungorum. Systematic assignment of plants tis Jacz. [Huseynova, 1961a]. Herbarium specimen was was performed based on APG IV system [APG IV, examined morphologically in this study, but not any 2016]. other structure characterizing genus Phyllactinia was 10 Aghayeva et al.: The genus Phyllactinia in Azerbaijan observed. Description of Ph. suffulta f. vitis provided identified asPh. fraxini. by B. Huseynova is quite similar to those of Ph. am- Ph. guttata (Wallr.: Fr.) Lév., Bot., 3 Sér., 15: 144, pelopsidis in 180–200 μm diameter of chasmothecia [in 1851; ≡ Ph. corylea (Pers.) P.Karst.; = Ph. suffulta f. monograph 150–280 μm], 6–8 number [5–14] and up to coryli-avellanae Jacz.; Host: Corylus avellana L., C. 250 μm length [250–370 μm] of acicular appendages, colurna L. (Betulaceae); BAK 5597–5601, 5637–5645, 54–76 × 22–30 μm [50–100 × 20–45 μm] and ellipsoid- 5648, 5650–5658; Distribution: Qusar, Khachmaz, ovoid, 2(–3)-spored of asci. However, Ph. suffulta f. Shabran, Shaki, Oghuz, Qakh, Zaqatala, Lankaran, vitis was given the affinity and status unclear taxa in Lerik, Shusha, Kalbajar, Askeran, Ordubad (Fig. 2.4). monograph of the Erysiphales [Braun, Cook, 2012], but Nowadays Erysiphe corylacearum U. Braun & S. this taxon was revised as Ph. ampelopsidis according to Takam. was recorded as a new powdery mildew patho- the description given in the literature. Additional col- gen on hazelnut in Azerbaijan and become well distrib- lections are required to clarify taxonomic status of this ute here [Abasova et al., 2018]. However, both surface species using molecular-phylogenetic and detail mor- of leaf, and nuts of hazelnut are became heavily infected phological approaches. by this pathogen, faint colonies of Ph. guttata also oc- Ph. babayanii Simonyan, Mikol. Fitapatol. 18(6): cur on the same leaves. Thus, now Ph. guttata coexists 465, 1984; = Ph. salmonii f. amygdali Babayan; Host: on the same host with E. corylacearum in the country. Prunus fenzliana Fritsch. (Rosaceae); BAK 5607; Dis- Ph. mali (Duby) U. Braun, Feddes Repert. 88(9– tribution: Julfa. 10): 657, 1978; ≡ Ph. mespili (Castagne) S. Blumer; = Ph. carpini (Rabenh.) Fuss, Arch. Ver. Sibenb. Ph. suffulta f. pruni Jacz., f. piri Jacz.; = Ph. guttata Landesk. 14(2): 463, 1878; = Ph. suffulta f. carpini- f. crataegi-oxyacanthae Sacc.; Host: Crataegus meyeri betuli Jacz.; Host: Carpinus betulus L. (Betulaceae); A.Pojark, C. monogyna Jacq., C. orientalis M.Bieb., C. BAK 5618–5623, 5627; Distribution: Qusar, Zaqatala, pentagyna Waldst. et Kit. ex Willd., Mespilus germani- Astara, Gadabay, Askeran. ca L., Pyrus communis L., P. salicifolia Pall., P. syriaca Ph. corni H.D.Shin & M.J.Park, Braun & Cook, 241, Boiss., Cerasus microcarpa (C.A.Mey.) Boiss. (Rosa- 2012; = Ph. suffulta f. corni Jacz.; Host: Cornus mas L., ceae); BAK 5602–5604, 5660, 5661, 5663, 5691–5697, C. sanguinea L. (Cornaceae); BAK 5628–5632, 5634, 5702–5709, 5711, 5712, 10027; Distribution: Baku, 5635, 5636; Distribution: Zaqatala, Balakan, Askeran, Shabran, Quba, Qusar, Zaqatala, Qazakh, Khojavend, Khojavend, Ordubad (Fig.2.2). Lerik, Shusha, Ordubad, Shahbuz. Ph. fraxini (DC.) Fuss, Arch. Ver. Siebenb. Landesk. Ph. marissalii (Westend.) U. Braun, Braun & Cook 14(2): 463, 1878; Host: Fraxinus excelsior L., F. sog- 262, 2012; = Ph. suffulta f. aceris Jacz.; Host: Acer diana Bunge (Oleaceae); BAK 5667–5677, 5679; Dis- platanoides L. (Sapindaceae); Distribution: Oghuz, Za- tribution: Qusar, Khachmaz, Absheron, Zaqatala, Lerik, qatala. Information about distribution of this fungus in Shusha, Khojavend, Ordubad (Fig.2.3). Two Phyllac- the country was given according in the Ibrahimov et al. tinia species, Ph. fraxini and Ph. fraxinocola U.Braun [1956]. But herbarium specimen of fungus was not de- & H.D.Shin were known on Fraxinus spp. worldwide posited in BAK. New collections are needed to confirm [Braun, Cook, 2012]. According to the monograph of distribution of this fungus in the country. the Erysiphales [Braun, Cook, 2012] there is not major Ph. moricola (Henn.) Homma, Trans. Sapporo Nat. differences in sexual morphs between these two spe- Hist. Soc. 11: 174, 1930; = Ph. suffulta f. moricola cies. Mainly they could be distinguished based on their Jacz.; Host: Morus alba L., M. australis Poir. (Morace- asexual structures [Scholler et al., 2018]. Specimens ae); BAK 5605, 5680–5688, 5690, 10032; Distribution: namely Ph. suffulta f. fraxini DC. collected in Azer- Absheron, Zaqatala, Ordubad (Fig. 2.5). baijan were in sexual stage. Therefore identification of Ph. nivea (Castagne) U. Braun, Braun & Cook 263, samples was done based on characteristics of sexual 2012; Host: Ulmus glabra Huds., U. minor Mill., U. structures, principally on asci. Asci with 2–4-spors are densa Litv. (Ulmaceae); BAK 5713–5717; Distribu- usual for both species, but 3–4-spored ones are frequent tion: Khojavend, Ordubad, Babek (Fig. 2.6). Informa- in Ph. fraxini, which was observed in our specimens. tion about distribution of this species in the country was Length of asci in our specimens varies between 70–101 given in monograph of the Erysiphales [Braun, Cook, μm, but it is 50–105 μm in Ph. fraxini and 50–90 μm in 2012]. But herbarium specimen of this fungus is not Ph. fraxinicola according to the Manual [Braun, Cook, stored in BAK. While, samples of Phyllactinia fungus 2012]. Based on these similarities our specimens were on Ulmus spp. collected in Azerbaijan were previously

11 Plant & Fungal Research identified as Ph. suffulta f. ulmi Jacz. and distribution applicable for morphological examination and there is of this fungus within the country reported in numerous not any other additional collection to proof the status of local literature [Akhundov, 1965; Huseynova, 1961b; this species. Ibrahimov et al., 1956]. Currently this taxon was re- Ph. populi (Jacz.) Y.N.Yu, in Yu & Lai, Acta Micro- named as Ph. angulata var. ulmi U. Braun based on biol. Sin. 19(1): 18, 1979; = Ph. suffulta f. populi Jacz.; modern taxonomic changes [Braun, Cook, 2012]. In Host: Populus sp. L. (Salicaceae); Distribution: Quba, morphological re-analysis of specimens of Ph. sufful- Zaqatala. Morphological description and information ta f. ulmi, clavate conidia in 33–72 × 18–22(–26) μm about distribution of this species were given according were observed. On whole, characteristics of sexual and to the local literature [Ibrahimov et al., 1956]. However, asexual morphs are in good agreement with Ph. nivea herbarium specimen was not deposited to BAK. by having clavate, 50–70 × 15–22 μm conidia [Braun, Ph. pyri-serotinae Sawada, Rep. Dept. Agric. Cook, 2012]. Whereas Ph. angulata var. ulmi is char- Gov. Res. Inst. Formosa 49:83, 1930; =Ph. suffulta acterized by its unique shape of conidia (dumb-bell- f. cotoneastri Jacz.; Host: Cotoneaster racemiflorus shape), which was not found in our specimens. There- (Desf.) C.Koch. (Rosaceae); BAK 5659; Distribution: fore, specimens previously reported as Ph. suffulta f. Shahbuz. ulmi were re-identified asPh. nivea. Ph. roboris (Gachet) S. Blumer, Beitr. Krypt-Fl. Ph. orbicularis (Ehrenb.) U. Braun, Braun & Cook Schweiz 7(1): 389, 193; Host: Quercus iberica M.Bieb., 264, 2012; Host: Fagus orientalis L. (Fagaceae); BAK Q. robur L. (Fagaceae); BAK 5606, 5616, Distribution: 5665; Distribution: Zaqatala (Fig. 2.7). Ph. suffulta f. Shusha, Ganja. Distribution of Ph. roboris on oak spe- fagi Duby was known on beech trees in Azerbaijan to cies in Azerbaijan was mentioned by Huseynov [Husey- date [Ibrahimov, 1956]. Information of this taxa was nov, 1988]. Fungus was collected in asexual stage from found neither in monograph of the Erysiphales [Braun, Ganja district. Besides, information about powdery Cook, 2012], nor in Index Fungorum. According to the mildew belonging to the genus Phyllactinia on Quercus morphological re-examination of specimen of Ph. suf- spp., which was identified as Ph. suffulta var. angulata fulta f. fagi, fungus was revised as Ph. orbicularis based (E.S. Salmon) Sacc. & Trotter given in some local man- on identity of sexual morphs in 150–190 μm diam. of uscripts [Huseynova 1961 a, b]. This fungus is men- chasmothecia [175–265 μm]; 6–12 [4–18] number of tioned as Ph. angulata (E.S. Salmon) S. Blumer var. acicular appendages; 54–72 × 26–30 μm size [(50–)60– angulata in Index Fungorum and this species is char- 95 × 25–45 μm] and having 2-spored asci. acterized by having dumb-bell-shaped conidia and en- Ph. paliuri U. Braun, Braun & Cook, 265, 2012; demic to North America. Two specimens of Ph. suffulta Host: Paliurus spina-christi Mill. (Rhamnaceae); BAK var. angulata were revised morphologically. Herbarium 5699, 5700; Distribution: Oghuz, Lankaran, Astara sample (BAK 5617) collected from Khojavend district (Fig. 2.8). Phyllactinia powdery mildew fungus on was re-examined and was identified as E. alphitoides thorn plants was reported as Ph. suffulta f. paliuri Sacc. (Griff. & Maubl.) U. Braun & S. Takam. in Azerbaijan, so far [Ibrahimov et al., 1956]. In Mono- Specimen (BAK 5616) collected from Shusha was graph [Braun, Cook, 2012] and Index Fungorum this in sexual stage and conidia were not found to proof the taxa was not mentioned. The fungus from specimens of taxonomic status of this species. Thus, the specimens of Ph. suffulta f. paliuri was re-identified as Ph. paliuri Ph. suffulta var. angulata were re-named as Ph. roboris. according to the morphological analysis. Thereby, the sum of Phyllactinia powdery mildews oc- Ph. phaseolina N. Ahmad, D.G. Agarwal & A.K. cupies 13% of all powdery mildew species in this coun- Sarbhoy, Mycotaxon 29: 68, 1987; =? Ph. suffulta f. try (Fig. 3), which is a little bit higher compared with viciae Guseinova; Host: Vicia sepium L. (Fabaceae); the percentage in the world (10%) (Fig. 4). BAK 5719; Distribution: Shusha. Fungi from the ge- Host range. In the current study, 32 plant species nus Phyllactinia are known as strictly woody parasitic from 12 families were recorded as hosts for the ge- plant pathogens worldwide. However, fungus was first nus Phyllactinia in Azerbaijan. This is only 5% of to- described on herbaceous plant (V. sepium) as Ph. suf- tal number of host plants for this genus in the world. fulta f. viciae in Azerbaijan [Huseynova, 1961] and cur- These families allocated among Asterids (Cornaceae, rently was renamed as Ph. phaseolina based on modern Oleaceae) and Rosids (Fabaceae, Betulaceae, Fagaceae, taxonomic changes [Braun, Cook, 2012]. This species Salicaceae, Moraceae, Rhamnaceae, Rosaceae, Ulma- is considered as doubtful, due to the type material is not ceae, Sapindaceae, Vitaceae) groups. Economically im-

12 Aghayeva et al.: The genus Phyllactinia in Azerbaijan

Figure 2.1. Phyllactinia alnicola on Alnus glutinosa (BAK 5612): A. chasmothecia; B,C. asci and ascospores; 2.2. Ph. corni on Cornus mas (BAK 5630): A. chasmothecia; B,C. asci and ascospores; 2.3. Ph. fraxini on Fraxinus excelsior (BAK 5670): A. chasmothecia; B, C. asci and ascospores; 2.4. Ph. guttata on Corylus avellana (BAK 5645): A. chasmothecia; B. ascus and ascospores; C. penicillate cells; 2.5. Ph. moricola on Morus australis (BAK 5685): A. chasmothecia; B, C. asci and ascospores; 2.6. Ph. nivea on Ulmus minor (BAK 5713): A. chasmothecia; B. ascus and ascospores; C. penicillate cells; 2.7. Ph. orbicularis on Fagus orientalis (BAK 5665): A. chasmothecia, B. acicular appendages with bulbous swelling; C. penicillate cells; D. asci and ascospores; 2.8. Ph. paliuri on Paliurus spina-christi (BAK 5700): A. ruptured casmothecia; B. acicular appendage with bulbous swelling; C, D, E. asci and ascospores; Bar = 100 μm.

13 Plant & Fungal Research

10% 13% 12

88% 6 90%

2 Number Number of plant species

0 Figure 3. Fungi from genus Phyllactinia within

all powdery mildew fungi in Azerbaijan: 88% all Plant families powdery mildew taxa; 13% Phyllactinia species. Figure 5. Allocation of host plant species among families.

13% 10% 10 9 8 7 88% 90% 6 5 4 3 Figure 4. Fungi from genus Phyllactinia within all Number of fungal taxa 2 1 powdery mildew fungi worldwide: 90% all powdery 0 Great Lower Lankaran Kur lowland Middle Araz mildew taxa; 10% Phyllactinia species. Caucasus Caucasus portant plant species, as fruits, medicinal, ornamental Figure 6. Geographical distribution of powdery mildews and forest trees are included in the hosts. among physic-geographical regions of Azerbaijan. Rosaceae composes the highest number of hosts (11 buz, Julfa, and Babek administrative divisions, which species) for two powdery mildew species from this ge- covers area belonging to the Nakhchivan Autonomous nus, followed by family Betulaceae, in which four plant Republic. In this region seven of the 17 Phyllactinia species are infected by three fungal taxa (Fig. 5). Ac- taxa were recorded. The west part of the country, which cording to the S. Takamatsu et al. [2008] special affinity situated on the Lesser Caucasus mountain range, has re- of Phyllactinia powdery mildews is to the hosts from cords of six from the 17 Phyllactinia taxa. Samples of family Betulaceae. Because the highest number of hosts these taxa were collected from Shusha, Gadabay, Ganja, from family Rosaceae does not definitely indicate their Askeran and Kalbajar districts of this region. special affinity to the genusPhyllactinia , essentially for The lower number of powdery mildew species were being of Rosaceae the large family within angiosperms. detected from regions Kur lowland and Lankaran, in It is noted that, species from genus Phyllactinia expand which each four fungal taxa were recorded for the re- their host range within a single family or genus [Taka- spective regions. Kur lowland covers central part of matsu et al., 2008], which is confirmed from our study, country, along the river Kur and Phyllactinia species too. were recorded from Qazakh, Khojavend and Balakan Geographical distribution. Study on geographical dis- districts. Samples of Phyllactinia were collected from tributions of Phyllactinia powdery mildews was carried districts Astara, Lerik, and Lankaran in the Lankaran out to reveal that these fungi are detected in mountainous region. Districts where the samples were reported are areas of five regions in Azerbaijan (Fig. 6). Of these five shown on the map (Fig. 7). regions, South-Eastern Great Caucasus region, which Ph. fraxini, Ph. guttata and Ph. mali are commonly covers north part of the country, has largest number distributed throughout Azerbaijan. Thus, these species (10 taxa) of Phyllactinia species. Absheron peninsula, were found in most of the 19 districts (Absheron, Baku, Quba, Qusar, Khachmaz, Shabran, Shaki, Oghuz, Qakh Quba, Qusar, Khachmaz, Shabran, Shaki, Oghuz, Qakh, and Zaqatala districts, from where powdery mildews Zaqatala, Lankaran, Lerik, Shusha, Kalbadgar, Asker- given in this study were recorded, belong to this region. an, Ordubad, Shahbuz, Khodgavand, Qazakh) from all Middle Araz region composed of the Ordubad, Shah- five regions. 14 Aghayeva et al.: The genus Phyllactinia in Azerbaijan

çağırışlar” adlı konfransın materialları, 20/21.05, Bakı, 111-113. (in Azerbaijani) Abasova L.V., Aghayeva D.N., Takamatsu S. (2018) Notes on powdery mildews of the genus Erysiphe from Azerbaijan. CREAM, 8(1): 30-53. Akhundov T.M. (1965) Muchnisto-rosyaniye qribi rodov Рhyllactinia, Sphaerotheca, Podosphaera Nakhichevanskoy ASSR. Izvestiye Akademii Nauk Azerbaidjanskoy SSR, seriya bioloqicheskikh nauk, 3: 24-33. (in Russian) Amano K. (1986) Host range and geographical distribution of the powdery mildew fungi. Japan Scientific Societies Press, Tokyo, 741 p. An update of the angiosperm phylogeny group clas- sification for the orders and families of flowering plants: APG IV (2016) Bot. J. Linn. Soc. 181: 1-20. Figure 7. Geographical distribution of powdery Braun U., Cook R.T.A. (2012) Taxonomic manual of mildews within Azerbaijan. the Erysiphales (Powdery mildews). CBS Biodi- versity series No. 11. Netherlands, Utrecht: CBS- CONCLUSIONS KNAW Fungal Biodiversity Centre, 707 p. This study examines diversity of Phyllactinia species in Glawe D.A. (2008) The powdery mildews: a review of Azerbaijan. Flora of the country is very rich in number the world’s most familiar (yet poorly known) plant of indigenous angiosperm species. About 900 powdery pathogens. Annu Rev Phytopathol, 1(12): 27-51. mildew species of Erysiphales were recorded on 10 Huseynova B.F. (1961a) Noviye I redko vstrechayush- thousand hosts worldwide [Braun, Cook, 2012; Amano, iesya vidi qribov sobranniye v Naqorna-Karabakhs- 1986]. Our recent studies reported 134 powdery mildew koy avtonomnoy oblasti. Izv. Akad. Azerb. SSR, ser. taxa on 420 plant species, which is 9% of all plant spe- biol. i med. nauk, 9: 3-9. (in Russian) cies, naturally growing in this country. Taking into ac- Huseynova B.F. (1961b) Nekotoriye danniye o vidovom count the rich flora and favorable condition for powdery sostove qribov Naqorna-Karabakhskoy avtonomnoy mildew infection in this country, much more new Phyl- oblasti. Izv. Akad. Azerb. SSR, ser. biol. i med. nauk, lactinia species and their new hosts are expected to be 12: 17-23. (in Russian) found in the future. Huseynov E.S. (1988) Sumchatiye qribi osnovnikh Consequently, herbarium samples of 14 taxa of the lesoobrazuyishikh porod Azerbaidjana. Izv. Akad. genus Phyllactinia are available in Mycological Her- Azerb. SSR, ser. biol. nauk, 5: 139-147. (in Russian) barium of Institute of Botany. The examined herbarium Ibrahimov H.R., Israfilbeyov L.A., Akhmadzade Z. samples were collected in different years, and most of (1956) Obzor nekotorikh vidov muchnisto-ro- them were useful for only morphological investigation syonikh qribov Azerbaidjana. Ucheniye zapiski of teleomorph and anamorph structures. New collec- Azerbaidjanskoy Qosudarstvennoy Universiteta, tions are needed for resolving intergeneric and inter- imeni S.M. Kirova, 6: 59-69. (in Russian) specific variability of Phyllactinia based on molecu- Kirk P. Index Fungorum. http://www.indexfungorum. lar analyses (DNA barcoding) by using genus specific org. primers. Further investigations are urgently required Meeboon J., Takamatsu S. (2015) Erysiphe takamatsui, to clarify the exact mycoflora of powdery mildews in a powdery mildew of lotus: Rediscovery of teleo- Azerbaijan. morph after 40 years, morphology and phylogeny. Mycoscience, 56: 159-167. REFERENCES Scholler M., Schmidt A., Meeboon J., Braun U., Taka- Abasova L.V., Ağayeva D.N. (2018) Azərbaycanda matsu S. (2018) Phyllactinia fraxinocola, another Erysiphales sırası göbələklərinin sahib bitkiləri. Asian fungal pathogen on Fraxinus excelsior (com- Azərbaycan Botaniklər Cəmiyyəti, V.C.Hacıyevin mon ash) introduced to Europe? Mycoscience, 59: 90 illiyinə həsr edilmiş “Botaniki tədqiqatlarda yeni 85-88.

15 Plant & Fungal Research

Shin H.D., La Y. (1993) Morphology of edge lines of alnicola, Ph. ampelopsidis, Ph. babayanii, Ph. carpini, chained immature conidia on conidiophores in pow- Ph. corni, Ph. fraxini, Ph. guttata, Ph. mali, Ph. ma- dery mildew fungi and their taxonomic significance. rissalii, Ph. moricola, Ph. nivea, Ph. orbicularis, Ph. Mycotaxon, 46: 445–451. paliuri, Ph. phaseolina, Ph. populi, Ph. pyri-serotinae Shin H.D., Lee H.J. (2002) Morphology of penicillate və Ph. roboris göbələkləri olaraq qeyd edilmişdir. Bitki cells in the genus Phyllactinia and its taxonomic ap- fəsilələri Asteridlər (Cornaceae, Oleaceae) və Rosidlər plication. Mycotaxon, 83: 301-325. (Fabaceae, Betulaceae, Fagaceae, Salicaceae, Morace- Takamatsu S. (2013) Molecular phylogeny reveals phe- ae, Rhamnaceae, Rosaceae, Ulmaceae, Sapindaceae, notypic evolution of powdery mildews (Erysiphales, Vitaceae) qruplarına daxil olub, bunlardan Rosidlər Ascomycota). J. Gen. Plant Pathol., 79: 218-226. qrupu sahib bitki sayına görə üstünlük təşkil edir. Onlar Takamatsu S., Inagaki M., Niinomi S., Khodaparast arasında Rosaceae fəsiləsinə aid növlərin üstünlük təşkil S.A., Shin H.D., Grigaliunaite B., Havrylenko M. etməsinə baxmayaraq, Phyllactinia cinsinin Betulaceae (2008) Comprehensive molecular phylogenetic fəsiləsinə aid bitkilərlə xüsusi yaxınlığının olması eh- analysis and evolution of the genus Phyllactinia timal edilir. Əlavə olaraq, bu cinsin nümayəndələrinin (Ascomycota: Erysiphales) and its allied genera. əsasən dağlıq ərazilərdə yayılmağa meylli olması Mycol. Res., 112: 299-315. müşahidə edilmişdir. Phyllactinia cinsinin daha çox say- Takamatsu S., Siahaan S.A.S., Moreno-Rico O., Ca- da nümayəndələri ölkənin Böyük Qafqazın cənub-şərq brera de Alvarez M.G., Braun U. (2016) Early evo- vilayətinə aid olan rayonlarından qeydə alınmışdır. Bu lution of endoparasitic group in powdery mildews: sıra Orta Araz və Kiçik Qafqaz vilayəti ilə davam edilir. molecular phylogeny suggests missing link between Ən az sayda göbələk növünə Kür dağarası çökəkliyi və Phyllactinia and Leveillula. Mycologia, 108(5): Lənkəran vilayətlərində qeydə alınmışdır. Tədqiqat işi 837-850. zamanı müəyyən edilmişdir ki, Phyllactinia cinsindən Vincent R., Duong V., Amor A., de Wiele N. (2013) olan 14 göbələk taksonuna aid herbari nümunələri BAK MycoBank gearing up for new horizons. IMA Fun- herbarisində mövcuddur və bu nümunələr haqqında gus, 4(2): 371-379, http://www.mycobank.org. məlumatlar məqalədə öz əksini tapmışdır. Açar sözlər: yayılma, ektoparazitizm, endoparazitizm, Azərbaycanda Phyllactinia sahib bitki, bitki patogeni, unlu şeh göbələyi (Ascomycota, Erysiphales) cinsinə ümumi baxış Обзор рода Phyllactinia Dilzarə N. Ağayeva (Ascomycota, Erysiphales) в Азербайджане Lamiya V. Abasova AMEA Botanika İnstitutu, Badamdar şossesi 40, Дильзара Н. Агаева Bakı, AZ1004, Azərbaycan Ламия В. Абасова Институт Ботаники НАНА, Бадамдар 40, Susumu Takamatsu Баку, AZ1004, Азербайджан Bioresurslar Məktəbi, Mie Universiteti, 1577 Kurima-Maçiya, Tsu 514-8507, Yaponiya Сусуму Такаматсу Школа Биоресурсов, Университет Мие, 1577 Azərbaycan Milli Elmlər Akademiyasının Botanika İns- Курима-Мация, Цу 514-8507, Япония titutunun Mikoloji herbarisində (BAK) saxlanılan və son illərdə toplanılan nümunələrin morfoloji yanaşmaların Изучено внутривидовое разнообразие мучнисто-ро- istifadəsi ilə təhlili əsasında Azərbaycanda Phyllactinia сяных грибов из рода Phyllactinia, встречающихся cinsi daxilində unlu şeh göbələklərinin növ müxtəlifliyi в Азербайджане. Повторно исследованы гербарные tədqiq edilmişdir. Ətraflı taksonomik təhlilin aparılma- образцы, хранящиеся в Микологическом гербарии sı üçün ədəbiyyat məlumatları da təftiş olunmuşdur. Института Ботаники (БАК) Национальной Акаде- Müasir taksonomik və nomenklatur dəyişiklər nəzərə мии Наук Азербайджана, и проанализированы вновь alınmışdır. Cinsə daxil olan göbələklərin sahib bitkiləri собранные в последние годы материалы с использо- və ölkə daxilində coğrafi yayılması aydınlaşdırılmışdır. ванием морфологических методов. Для проведения Nəticədə, 17 unlu şeh göbələyi taksonu aşkar edilmişdir детального таксономического анализа были пере- ki, bunlar 11 fəsilədən olan 32 növ bitki üzərində Ph. смотрены имеющиеся литературные данные и учте- ны современные таксономические и номенклатур- 16 Aghayeva et al.: The genus Phyllactinia in Azerbaijan

ные изменения. Был выяснен ряд растений хозяев тений-хозяев, считается, что род Phyllactinia по и определено географическое распространение гри- специфическому родству скорее ближе к растени- бов из рода Phyllactinia в регионах Азербайджана. В ям из семейства Betulaceae. Было обнаружено, что итоге зарегистрировано распространение 17 таксо- грибы из рода Phyllactinia имеют склонность к рас- нов мучнисто-росяных грибов из данного рода, из пространению в основном в горных районах Азер- которых Ph. alnicola, Ph. ampelopsidis, Ph. babayanii, байджана. Наибольшее количество представителей Ph. carpini, Ph. corni, Ph. fraxini, Ph. guttata, Ph. mali, рода Phyllactinia было зафиксировано в районах Ph. marissalii, Ph. moricola, Ph. nivea, Ph. orbicularis, Азербайджана, относящихся к южно-восточной об- Ph. paliuri, Ph. phaseolina, Ph. populi, Ph. pyri- ласти Большого Кавказа. Области Средний Араз и serotinae и Ph. roboris были перечислены на 32 ви- Малый Кавказ следует за ним. Наименьшее количе- дах растений, относящихся к 11 семействам. Эти се- ство грибов Phyllactinia зафиксировано в Куринской мейства относятся к группам Астеридов (Cornaceae, межгорной впадине и Лянкяранском области. В ходе Oleaceae) и Розидов (Fabaceae, Betulaceae, Fagaceae, исследования выявлено, что 13 гербарных образцов Salicaceae, Moraceae, Rhamnaceae, Rosaceae, рода Phyllactinia, о которых приведена информация Ulmaceae, Sapindaceae, Vitaceae), причем группа в данной статье, имеются в БАК. Розидов по количеству видов превышает число ви- Ключевые слова: распространение, эктопарази- дов хозяев. Несмотря на то, что семейство Rosaceae тизм, эндопаразитизм, растение-хозяин, расти- обладает самым большим количеством видов рас- тельный патоген, мучнистая роса